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Evolutionary Genomics Revealed Interkingdom Distribution of Tcn1

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Evolutionary Genomics Revealed Interkingdom Distribution of Tcn1 Novikova et al. BMC Genomics 2010, 11:231 http://www.biomedcentral.com/1471-2164/11/231 RESEARCH ARTICLE Open Access EvolutionaryResearch article genomics revealed interkingdom distribution of Tcn1-like chromodomain-containing Gypsy LTR retrotransposons among fungi and plants Olga Novikova*1, Georgiy Smyshlyaev2 and Alexander Blinov1 Abstract Background: Chromodomain-containing Gypsy LTR retrotransposons or chromoviruses are widely distributed among eukaryotes and have been found in plants, fungi and vertebrates. The previous comprehensive survey of chromoviruses from mosses (Bryophyta) suggested that genomes of non-seed plants contain the clade which is closely related to the retrotransposons from fungi. The origin, distribution and evolutionary history of this clade remained unclear mainly due to the absence of information concerning the diversity and distribution of LTR retrotransposons in other groups of non-seed plants as well as in fungal genomes. Results: In present study we preformed in silico analysis of chromodomain-containing LTR retrotransposons in 25 diverse fungi and a number of plant species including spikemoss Selaginella moellendorffii (Lycopodiophyta) coupled with an experimental survey of chromodomain-containing Gypsy LTR retrotransposons from diverse non-seed vascular plants (lycophytes, ferns, and horsetails). Our mining of Gypsy LTR retrotransposons in genomic sequences allowed identification of numerous families which have not been described previously in fungi. Two new well-supported clades, Galahad and Mordred, as well as several other previously unknown lineages of chromodomain-containing Gypsy LTR retrotransposons were described based on the results of PCR-mediated survey of LTR retrotransposon fragments from ferns, horsetails and lycophytes. It appeared that one of the clades, namely Tcn1 clade, was present in basidiomycetes and non-seed plants including mosses (Bryophyta) and lycophytes (genus Selaginella). Conclusions: The interkingdom distribution is not typical for chromodomain-containing LTR retrotransposons clades which are usually very specific for a particular taxonomic group. Tcn1-like LTR retrotransposons from fungi and non- seed plants demonstrated high similarity to each other which can be explained by strong selective constraints and the 'retained' genes theory or by horizontal transmission. Background rotransposons are divided into several superfamilies: Retrotransposons are a class of mobile genetic elements, Copia (Pseudoviridae), Gypsy (Metaviridae), Bel-Pao, which use reverse transcription in their transposition. Retrovirus (Retroviridae), and ERV [1]. Five orders of retrotransposons are recognized: those Chromodomain-containing LTR retrotransposons or having long terminal repeats (LTRs) (LTR retrotranspo- chromoviruses are the most widespread lineage of Gypsy sons); those lacking LTRs (non-LTR retrotransposons); LTR retrotransposons and are present in genomes of DIRS retrotransposons; Penelope-like retrotransposable fungi as well as in plants and vertebrates [2,3]. The char- elements; and short interspersed nuclear elements acteristic feature of chromoviruses is the presence of an (SINEs). According to the modern classification, LTR ret- additional domain - the chromodomain (CHD). CHDs are present in various eukaryotic proteins involved in * Correspondence: [email protected] chromatin remodeling and regulation of gene expression 1 Laboratory of Molecular Genetic Systems, Institute of Cytology and Genetics, Novosibirsk, Russia during development [4-6]. CHDs perform a wide range of Full list of author information is available at the end of the article © 2010 Novikova et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons BioMed Central Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Novikova et al. BMC Genomics 2010, 11:231 Page 2 of 20 http://www.biomedcentral.com/1471-2164/11/231 diverse functions including chromatin targeting and pro- in mosses (Bryophyta) [8]. The survey was performed teinDNA/RNA interactions [6]. Recently, it has been using genome sequence data for the 25 fungal species shown that the CHDs target integration of new LTR ret- listed in Table 1. The hemiascomycetous yeasts were not rotransposon copies into heterochromatin by recognizing included in the present investigation since a comprehen- histone modifications [7]. sive survey of LTR retrotransposons from this group of Our previous comprehensive survey of chromoviruses ascomycetes was recently published [10]. First, reverse from mosses (Bryophyta) suggested that the diversity of transcriptase (RT) and integrase (Int) coding regions of CHD-containing Gypsy LTR retrotransposons in plant Gypsy LTR retrotransposons were detected in genomic genomes is underestimated [8,9]. There are four well- sequences using algorithm based on hidden Markov known CHD-containing Gypsy LTR retrotransposon model implemented in uGENE software http:// clades widely distributed among gymnosperms and ugene.unipro.ru/. The transposable elements thus identi- angiosperms: Tekay, CRM, Galadriel and Reina [2,3]. fied were then classified into families based on RT and Int Four novel clades were found to be present in mosses. domains sequence similarity. Members of the same fam- Moreover, we showed that representatives from one of ily shared high amino acid identity (90-100%) but had the moss-specific clades are more closely related to ret- very little similarity to elements from other families. Our rotransposons from fungi than to retrotransposons from survey has identified more than 150 novel Gypsy LTR ret- plants. Although we proposed that the retrotransposons rotransposon families which have not been described from this clade could have been 'retained' from the last previously (Additional file 1). common ancestor of Fungi/Metazoa lineage and plants, The newly identified Gypsy LTR retrotransposons fall the origin of this clade remains unclear. into two major, distinct lineages according to phyloge- The questions addressed in current investigation are as netic analysis based on RT and partial Int domains: chro- follows: (1) what kind of Gypsy LTR retrotransposons moviruses (or CHD-containing Gypsy LTR from fungi are closely related to the LTR retrotranspo- retrotransposons) and Ylt1-like LTR retrotransposons. sons detected in mosses; (2) how widely those clades Two retrotransposons (LacBicTy3-15 from Laccaria which were previously identified in mosses are distrib- bicolor and CopConTy3-14 from Coprinus cinereus) uted among other non-seed plants including lycophytes, formed their own lineage closely related to Ylt1-like LTR ferns and horsetails; and (3) what is the origin of the clade retrotransposons. This lineage cannot be attributed to which is common for non-seed plants and fungi. The in Ylt1 because of low bootstrap support (only 64%; Figure silico analysis of Gypsy LTR retrotransposons in 25 spe- 1) and was named SN_1006. Ylt1-like LTR retrotranspo- cies of fungi, genomes of which available in public data- sons were found in a number of fungal species (Figure 1). bases, along with survey of related LTR retrotransposons Previously, Ylt1-like LTR retrotransposons were reported from whole genome sequences (WGS) and expressed for Yarrowia lipolytica (original Ylt1 retrotransposon) sequence tags (ESTs) of diverse plants including spike- [11], Candida albicans (Tca3 element) [12], and basidio- moss Selaginella moellendorffii (Lycopodiophyta) and mycete Cryptococcus neoformans [13]. In the present PCR-based screening of ferns, horsetails and lycophytes study, LTR retrotransposons belonging to the Ylt1 lineage showed that a common clade of CHD-containing Gypsy have been found in both ascomycete and basidiomycete LTR retrotransposons can be found in mosses, lycophytes fungi. They fall into several clearly separated groups: the from genus Selaginella, and basidiomycetes. According to branch formed by transposable elements from Basidio- the classification of CHD-containing Gypsy LTR ret- mycota, the group of retrotransposons from ascomycetes, rotransposons proposed by Gorinsek et al. (2004) [3] this and the branch of the original Ylt1 LTR retrotransposon clade has name Tcn1. It seems that Tcn1 is a unique clade (Figure 1). of chromoviruses which has a wide inter-kingdom distri- Twenty monophyletic clades can be recognized in the bution. Tcn1-like LTR retrotransposons from fungi and phylogenetic tree of fungal CHD-containing Gypsy LTR non-seed plants demonstrated higher similarity to each retrotransposons, nine of which have been previously other in comparison with LTR retrotransposons from reported [3]. Thirteen clades are specific for ascomycetes other clades. This can be explained by strong selective (Nessie, Pyret, Maggy, Pyggy, MGLR3, Yeti, Coccy1, constraints and the 'retained' genes theory or by horizon- Coccy2, Polly, Afut1, Tf1, Ty3, and Afut4), six have been tal transmission. found only in genomes of basidiomycetes (MarY1, Laccy1, Laccy2, Tcn2, Puccy1, and Puccy2) and one clade Results (Tcn1) is present in both basidiomycetes and chytridio- Gypsy LTR retrotransposons survey from fungal genomes mycetes (Batrachochytrium dendrobatidis JEL423) (Fig- The Gypsy LTR retrotransposons mining from fungal ure 2). genomes was initiated in an attempt to identify ret- For each of the newly identified retrotransposon fami- rotransposons
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